Effects of structural memory in protein reactions

Abstract

Specific effects of the coupling of protein reactions to slow protein structure dynamics are studied. We focus on accumulation of structural changes produced in consecutive protein cycles and eventually modifying the cycle itself. We showed previously [Christophorov et al., Chem. Phys. 256, 45 (2000); Goushcha et al., Biophys. J. 79, 1273 (2000)] that such an effective interaction between cycles can cause the thresholdlike emergence of a new stable functional state of the protein macromolecule. To elucidate this mechanism, we have performed numerical modeling of the reaction kinetics in a two-state system coupled to diffusion in the corresponding conformational potentials. Specifically, the model is related to the charge separation and recombination processes in photosynthetic reaction centers (RCs). It is shown that the percentage of RCs remaining structurally deformed after recombination, until the next photoexcitation event (“memory-bearing” centers), can be quite low. Nonetheless, under prolonged photoexcitation it is sufficient for driving eventually all the RCs to a state of high charge-separation efficiency. The dependence of this efficiency on quasistationary photoexcitation intensity is pronouncedly hysteretic. The conformation potentials anharmonicity extends the bistability range noticeably, thereby improving RC adaptation properties. Experimental protocols to detect the memory-bearing centers in the RC ensemble are proposed, simulated and tested, disqualifying the electron escape to hypothetical redox traps. The technique proposed can be used in the studies of cooperative effects under repeated cycling of biomolecules.

Light-Induced Equilibration Kinetics in Membrane-Bound Photosynthetic Reaction Centers: Nonlinear Dynamic Effects in Multiple Scattering Media

“…These observations are quite different from what one obtains for isolated RCs under similar illumination conditions. 1,21 In analogous experiments with isolated RCs, the bleaching amplitude at 865 nm showed a pronounced dependence on the actinic light intensity over the entire photoexcitation intensity range. See Figure 2a.…”

“…The rate of electron recombination from the secondary quinone acceptor Q B is written in eq 1 as k r (x) ) k AP e -x . Such a dependence for RCs has been discussed in details previously 1,2,19,20,22 and was based on the fact that the rate constant of electron transfer from Q B to P at normal physiological conditions is given by By assumption that we obtain the assumed expression for k r (x). In the above consideration, we took into account that the slow component of structural rearrangements, triggered by electron localization on Q B causes slow changes in the ∆G AB value due to interaction with the polar surroundings of the secondary electron acceptor in RCs.…”

“…The calculation of RC absorption changes with variation of actinic light intensity is based on the model previously described for a reduced two-level scheme of RC redox states 1,2,19,20 in which P P (t,x) and P B (t,x) describe the time evolution of the RC distribution function over a single dimensionless structural variable x for two different redox states, PQ A Q B (neutral state) and P + Q A Q B -(charge separated state), respectively. I is the photoexcitation intensity, in units of single RC photoexcitations, and k AP is the rate of electron recombination from the primary quinone acceptor Q A to the bacteriochlorophyll dimer P. In eq 1 D i is the diffusion constant, ∆G AB is the difference of the quasi-free energies for electron localization on Q A and on Q B , k B is the Boltzmann constant, T is an absolute temperature, V P and V B are the redox potentials in units of k B T 1,2 in which γ i and R i < 1 are the anharmonicity parameters, and x P and x B are the minimum positions for the charge neutral…”

“…The structural diffusion constant of the charge neutral state was determined to be among the main parameters responsible for the emergence of a slow relaxation component in the kinetics of isolated RCs. 1,2 Despite the obvious interest in a comparison of results from studies of nonequilibrium dynamic effects in isolated RCs with those in chromatophores, the latter studies have not previously been performed because of apparent difficulties in deducing an unambiguous interpretation of the results of light-induced effects on photosynthetic membranes. The interpretation of experimental results on the dynamics of membrane-bound RCs is confounded by significant overlap of RC absorption with that of antennae complexes in these systems.…”

“…[1][2][3] In particular, a pronounced, slow relaxation phase following flash excitation is prominent in the equilibration kinetics of RCs isolated from the purple bacteria Rhodobacter (Rb.) sphaeroides after dialysis against an excess of two different detergents, either Triton X-100 (0.05%, pH 7.5) or sodium (Na) cholate (0.1%, pH 8.0).…”